Human skeletal muscle metabolic responses to 6 days of high‐fat overfeeding are associated with dietary n‐3PUFA content and muscle oxidative capacity
Abstract Understanding human physiological responses to high‐fat energy excess (HFEE) may help combat the development of metabolic disease. We aimed to investigate the impact of manipulating the n‐3PUFA content of HFEE diets on whole‐body and skeletal muscle markers of insulin sensitivity. Twenty he...
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Online Access: | https://doi.org/10.14814/phy2.14529 |
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doaj-f281b373384c4bcfa1f234ed1090cf252020-11-25T03:49:16ZengWileyPhysiological Reports2051-817X2020-08-01816n/an/a10.14814/phy2.14529Human skeletal muscle metabolic responses to 6 days of high‐fat overfeeding are associated with dietary n‐3PUFA content and muscle oxidative capacitySophie L. Wardle0Lindsay S. Macnaughton1Chris McGlory2Oliver C. Witard3James R. Dick4Philip D. Whitfield5Arny A. Ferrando6Robert R Wolfe7Il‐Young Kim8D. Lee Hamilton9Colin N. Moran10Kevin D. Tipton11Stuart D. R. Galloway12Physiology, Exercise and Nutrition Research Group University of Stirling Stirling UKPhysiology, Exercise and Nutrition Research Group University of Stirling Stirling UKPhysiology, Exercise and Nutrition Research Group University of Stirling Stirling UKPhysiology, Exercise and Nutrition Research Group University of Stirling Stirling UKNutrition Group, Institute of Aquaculture University of Stirling Stirling UKLipidomics Research Facility, Division of Biomedical Sciences University of the Highlands and Islands Inverness UKDepartment of Geriatrics, Center for Translational Research in Aging and Longevity Donald W. Reynolds Institute on Aging Little Rock AR USADepartment of Geriatrics, Center for Translational Research in Aging and Longevity Donald W. Reynolds Institute on Aging Little Rock AR USADepartment of Geriatrics, Center for Translational Research in Aging and Longevity Donald W. Reynolds Institute on Aging Little Rock AR USAPhysiology, Exercise and Nutrition Research Group University of Stirling Stirling UKPhysiology, Exercise and Nutrition Research Group University of Stirling Stirling UKPhysiology, Exercise and Nutrition Research Group University of Stirling Stirling UKPhysiology, Exercise and Nutrition Research Group University of Stirling Stirling UKAbstract Understanding human physiological responses to high‐fat energy excess (HFEE) may help combat the development of metabolic disease. We aimed to investigate the impact of manipulating the n‐3PUFA content of HFEE diets on whole‐body and skeletal muscle markers of insulin sensitivity. Twenty healthy males were overfed (150% energy, 60% fat, 25% carbohydrate, 15% protein) for 6 d. One group (n = 10) received 10% of fat intake as n‐3PUFA rich fish oil (HF‐FO), and the other group consumed a mix of fats (HF‐C). Oral glucose tolerance tests with stable isotope tracer infusions were conducted before, and following, HFEE, with muscle biopsies obtained in basal and insulin‐stimulated states for measurement of membrane phospholipids, ceramides, mitochondrial enzyme activities, and PKB and AMPKα2 activity. Insulin sensitivity and glucose disposal did not change following HFEE, irrespective of group. Skeletal muscle ceramide content increased following HFEE (8.5 ± 1.2 to 12.1 ± 1.7 nmol/mg, p = .03), irrespective of group. No change in mitochondrial enzyme activity was observed following HFEE, but citrate synthase activity was inversely associated with the increase in the ceramide content (r=−0.52, p = .048). A time by group interaction was observed for PKB activity (p = .003), with increased activity following HFEE in HF‐C (4.5 ± 13.0mU/mg) and decreased activity in HF‐FO (−10.1 ± 20.7 mU/mg) following HFEE. Basal AMPKα2 activity increased in HF‐FO (4.1 ± 0.6 to 5.3 ± 0.7mU/mg, p = .049), but did not change in HF‐C (4.6 ± 0.7 to 3.8 ± 0.9mU/mg) following HFEE. We conclude that early skeletal muscle signaling responses to HFEE appear to be modified by dietary n‐3PUFA content, but the potential impact on future development of metabolic disease needs exploring.https://doi.org/10.14814/phy2.14529exercisefish oilinsulin resistanceomega‐3overfeedingtype 2 diabetes |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Sophie L. Wardle Lindsay S. Macnaughton Chris McGlory Oliver C. Witard James R. Dick Philip D. Whitfield Arny A. Ferrando Robert R Wolfe Il‐Young Kim D. Lee Hamilton Colin N. Moran Kevin D. Tipton Stuart D. R. Galloway |
spellingShingle |
Sophie L. Wardle Lindsay S. Macnaughton Chris McGlory Oliver C. Witard James R. Dick Philip D. Whitfield Arny A. Ferrando Robert R Wolfe Il‐Young Kim D. Lee Hamilton Colin N. Moran Kevin D. Tipton Stuart D. R. Galloway Human skeletal muscle metabolic responses to 6 days of high‐fat overfeeding are associated with dietary n‐3PUFA content and muscle oxidative capacity Physiological Reports exercise fish oil insulin resistance omega‐3 overfeeding type 2 diabetes |
author_facet |
Sophie L. Wardle Lindsay S. Macnaughton Chris McGlory Oliver C. Witard James R. Dick Philip D. Whitfield Arny A. Ferrando Robert R Wolfe Il‐Young Kim D. Lee Hamilton Colin N. Moran Kevin D. Tipton Stuart D. R. Galloway |
author_sort |
Sophie L. Wardle |
title |
Human skeletal muscle metabolic responses to 6 days of high‐fat overfeeding are associated with dietary n‐3PUFA content and muscle oxidative capacity |
title_short |
Human skeletal muscle metabolic responses to 6 days of high‐fat overfeeding are associated with dietary n‐3PUFA content and muscle oxidative capacity |
title_full |
Human skeletal muscle metabolic responses to 6 days of high‐fat overfeeding are associated with dietary n‐3PUFA content and muscle oxidative capacity |
title_fullStr |
Human skeletal muscle metabolic responses to 6 days of high‐fat overfeeding are associated with dietary n‐3PUFA content and muscle oxidative capacity |
title_full_unstemmed |
Human skeletal muscle metabolic responses to 6 days of high‐fat overfeeding are associated with dietary n‐3PUFA content and muscle oxidative capacity |
title_sort |
human skeletal muscle metabolic responses to 6 days of high‐fat overfeeding are associated with dietary n‐3pufa content and muscle oxidative capacity |
publisher |
Wiley |
series |
Physiological Reports |
issn |
2051-817X |
publishDate |
2020-08-01 |
description |
Abstract Understanding human physiological responses to high‐fat energy excess (HFEE) may help combat the development of metabolic disease. We aimed to investigate the impact of manipulating the n‐3PUFA content of HFEE diets on whole‐body and skeletal muscle markers of insulin sensitivity. Twenty healthy males were overfed (150% energy, 60% fat, 25% carbohydrate, 15% protein) for 6 d. One group (n = 10) received 10% of fat intake as n‐3PUFA rich fish oil (HF‐FO), and the other group consumed a mix of fats (HF‐C). Oral glucose tolerance tests with stable isotope tracer infusions were conducted before, and following, HFEE, with muscle biopsies obtained in basal and insulin‐stimulated states for measurement of membrane phospholipids, ceramides, mitochondrial enzyme activities, and PKB and AMPKα2 activity. Insulin sensitivity and glucose disposal did not change following HFEE, irrespective of group. Skeletal muscle ceramide content increased following HFEE (8.5 ± 1.2 to 12.1 ± 1.7 nmol/mg, p = .03), irrespective of group. No change in mitochondrial enzyme activity was observed following HFEE, but citrate synthase activity was inversely associated with the increase in the ceramide content (r=−0.52, p = .048). A time by group interaction was observed for PKB activity (p = .003), with increased activity following HFEE in HF‐C (4.5 ± 13.0mU/mg) and decreased activity in HF‐FO (−10.1 ± 20.7 mU/mg) following HFEE. Basal AMPKα2 activity increased in HF‐FO (4.1 ± 0.6 to 5.3 ± 0.7mU/mg, p = .049), but did not change in HF‐C (4.6 ± 0.7 to 3.8 ± 0.9mU/mg) following HFEE. We conclude that early skeletal muscle signaling responses to HFEE appear to be modified by dietary n‐3PUFA content, but the potential impact on future development of metabolic disease needs exploring. |
topic |
exercise fish oil insulin resistance omega‐3 overfeeding type 2 diabetes |
url |
https://doi.org/10.14814/phy2.14529 |
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